THE PHYSIOLOGICAL IMPACT OF WOOL-HARVESTING PROCEDURES IN VICUNAS (VICUGNA VICUGNA) C Bonacic*† and D W Macdonald* * Wildlife Conservation Research Unit, University of Oxford, Department of Zoology, South Parks Road, Oxford OX1 3PS, UK † Departamento de Ciencias Animales, Facultad de Agronomia e Ingenieria Forestal, Pontificia Universidad Católica de Chile, Casilla 306, Correo 22, Santiago, Chile † Contact for correspondence and requests for reprints:
[email protected]
Abstract
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A current programme of wildlife utilisation in the Andean region involves the capture of wild vicunas, their shearing, transport and, in some cases, captive farming. The effects of these interventions on the physiology, and thus welfare, of wild vicunas are unknown. As a first step to quantifying and thus mitigating any adverse welfare consequences of this harvest, we measured the immediate and longer-term physical and physiological effects of capture, shearing and transport. A sample of juvenile male vicunas was captured. Six were shorn at the capture site, six after two weeks in captivity, and the remaining seven animals were kept as controls for 39 days. In general, vicunas showed changes in blood glucose, packed cell volume, cortisol, and neutrophil:lymphocyte ratios within 4–6 h following capture. Creatine kinase was also affected by capture and transport, showing a peak plasma level 24 h after capture, which was followed by a peak plasma level of aspartate aminotransferase four days after capture and transport. After 12 days in captivity, all of the vicunas showed physiological parameters close to expected baseline values for the species. We could detect no differences in physiological parameters between animals that were captured, sheared and transported and those that were only captured and transported. Similarly, we could detect no differences in most responses of vicunas between those sheared after 12 days in captivity and a control group held under similar conditions but from which blood was sampled without shearing. A further comparison between animals sheared immediately after capture and animals sheared after 12 days in captivity revealed that creatine kinase levels were higher in the former group. During transport prior to release back into the wild, only minor injuries (lip bleeding and limb contusions) and a significant increase in rectal temperature were observed. Our results provide a basis for recommendations to improve the welfare of vicunas during the wool harvest, and provide baseline and stress-response data to serve as reference points for further studies of vicuna welfare. Keywords: animal welfare, capture effects, ecophysiology, shearing effects, stress response, sustainable use Introduction The vicuna (or vicuña, Vicugna vicugna), a wild South American Camelid, is regularly captured, handled and sheared, and this practice has occurred since the 15th century, when the Inca Empire conducted a round-up, known as the chaku, throughout the Andes of South America (Hurtado 1987; Torres 1992). The chaku involved herding thousands of animals into stone corrals for shearing. Large numbers of animals were shorn using this method; © 2003 UFAW, The Old School, Brewhouse Hill, Wheathampstead, Herts AL4 8AN, UK
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probably whatever morbidity and mortality resulted (and there are no records of this) had little effect on the population because the chaku took place in a given locality only once every four years. Furthermore, prior to the arrival of Europeans, vicunas were abundant in the Andes (Koford 1957; Hurtado 1987). When Europeans arrived in South America, the traditional chaku was replaced by indiscriminate hunting (Hoffmann et al 1983; Cueto et al 1985; Hurtado 1987; CONAF 1991). The number of vicunas rapidly declined, probably through the combined impact of hunting, livestock competition and, possibly, diseases introduced by European domestic livestock (Koford 1957). By the 1950s the species faced extinction, but their decline was successfully reversed by the introduction of a 30-year moratorium (Bonacic et al 2002). Local communities observed this moratorium — enduring the loss of vicuna wool and meat, and tolerating perceived competition with livestock — in the expectation that they would see long-term benefits from the sustainable use of vicuna wool, a luxury product that attracts a high premium on international markets. Attempts to realise this potential market rest, under the dictates of CITES, on in vivo harvest of the vicuna’s wool. Clearly, this might be achieved by various means and, in evaluating the alternatives, one consideration is the welfare of the animals. Here, we report on our assessment of the welfare consequences of various aspects of the harvest. Current policies for vicuna management include capture and shearing of wild animals, farming, ranching, translocation and reintroduction (Cueto et al 1985; Torres 1987; Urquieta & Rojas 1990; Torres 1992; Rebuffi 1993; Urquieta et al 1994; Wheeler & Hoces 1997; Galaz 1998). For example, during the early 1990s, wild vicunas were translocated, by road and air, from Peru, Argentina and Chile to a Natural Reserve in Ecuador to begin a reintroduction programme (CITES 1997). The welfare implications of the handling and transportation of domestic stock are a longstanding topic of research (Goddard et al 1996; Grigor et al 1997a; Grigor et al 1997b). Although less scientific attention has been given to welfare as an element of wildlife conservation and management, it is already clear that capture and transportation can cause stress in wild ungulates as well as in carnivores and birds (Bailey et al 1996; DeNicola & Swihart 1997; Grigor et al 1998; Little et al 1998). In ungulates such as red deer (Cervus elaphus) and white-tailed deer (Odocoileus virginianus), capture and immobilisation are known to cause stress, as indicated by changes in haematological and biochemical blood constituents (Wesson et al 1979; Vassart et al 1992; Beringer et al 1996; DeNicola & Swihart 1997; Marco et al 1998). Specifically, capture and restraint can cause capture myopathy, also named exertional myopathy (for a review, see Wesson et al 1979; Beringer et al 1996; Williams & Thomas 1996; DeNicola & Swihart 1997). Capture myopathy is caused by complex metabolic changes that may result in hyper-acute fatal acid–base and electrolyte imbalances (Fowler 1998). Various biological and haematological parameters are known to vary according to the capture method, species and previous capture experience (Morton et al 1995). Capture myopathy is a syndrome resulting from excessive exercise and multiple traumas during capture and handling that produces dramatic changes in the activity of creatine kinase, aspartate aminotransferase, packed cell volume and cortisol (Radostits et al 1994). Interpretation of the physiological response to capture requires caution because of variation with age, season and, notably, species (see Bonacic et al, pp 369–385, this issue). However, it is generally true that capture induces, within seconds, changes in core body temperature (reflected by rectal temperature), catecholamine concentrations, heart rate, 388
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respiratory rate and packed cell volume (Eckert & Randall 1983; Schmidt-Nielsen 1997; Radostits et al 1994; Harris et al 1999). A less acute response (ie from minutes to hours) is observed in blood glucose, plasma cortisol and creatine kinase concentrations (Coles 1980; Kaneko et al 1997; Bateson & Wise 1998; Harris et al 1999). Finally, some parameters change only on a time-scale of hours to days, such as aspartate aminotransferase, total protein, and blood urea nitrogen (Kaneko et al 1997; Harris et al 1999). In the case of vicunas, our concern was that capture and shearing — activities essential to the planned sustainable harvest of wool — could result in morbidity and potential mortality; indeed, shearing is known to cause a risk of fatal hypothermia in other South American Camelids (Fowler 1998). Adverse signs of shearing in llamas (as in sheep) include decreased heart and respiratory rates, hypothermia and an increase in packed cell volume, accompanied by hypotension and a state of physical depression or lack of activity (Radostits et al 1994; Fowler 1998). Various capture, transport and shearing methods are currently used for vicunas throughout South America. The simplest capture method, in Peru, emulates the ancient chaku and involves people slowly herding groups of between 20 and 500 vicunas into a wire-fenced corral (Wheeler & Hoces 1997). Elsewhere, and commonly in Chile, motorbikes and pickups are used to drive small groups of animals for up to five kilometres into fenced corrals (Bonacic 2000). Some people use combinations of these approaches. Once in the corral, the vicunas are either restrained with ropes until they are shorn or wait unrestrained in an adjacent corral. The purpose of this study was to investigate the effects of different capture and handling strategies on selected physiological parameters. Here, we report on an experiment designed to disentangle the characteristics and relative magnitudes of physiological indicators of stress associated with each of a) capture, b) shearing, and c) transportation, and the effects of habituation on the vicuna’s response to stress. We provide capture and handling recommendations that optimise animal welfare and thus also maximise harvest sustainability. Methods Study area The study took place in Las Vicunas National Reserve (209 131 ha; South 18°16'–19°00' and West 68°57'–69°27') in Chile, which lies within the Surire basin in the Parinacota Province (490 401 ha) and has been used as a centre for research on the sustainable use of the vicuna (CONAF 1991). Rainfall (annual mean 200–321 mm) is concentrated in summer (December–March); July is the coldest month with a mean temperature of –0.04°C, and January the warmest with a mean of 8°C. The study was conducted in November 1998. Experimental design Vicunas were captured at Site Number 32 within The Las Vicunas National Reserve in the northern region of Chile at 4400 m above sea level, in an open grassland plain with steppe vegetation surrounded by mountains and bisected by a main road. Capture facilities were built at the middle of the site, 100–200 m east of a road. In the course of local shearing operations, 19 juvenile male vicunas were herded by vehicles into a corral (15 m × 25 m). Some were shorn immediately with mechanical clippers (Lister®) used for sheep. However, because vicunas are less tractable than sheep, shearing involved two people holding the animal prostrate on the ground (one at its head holding the forelegs, the other to the rear and holding the hindlegs), while a third person sheared the animal’s back and flanks. All of the vicunas, whether shorn or not, were then transported carefully in a Toyota double-cabin Animal Welfare 2003, 12: 387-402
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four-wheel-drive pick-up truck for 20 km at 40–50 km h–1 on a dirt road within the Reserve to the holding facility, where they were kept for 39 days (until 30 November 1998). The animals were transported in the same way after the study was completed, and clinical examination and any injuries during transport were recorded. Physical examination and blood sampling were carried out after capture, after transport to the capture facilities, and after shearing. The vicunas were allocated at random to one of three treatments: a) C-T: controls animals which were maintained in captivity but were not shorn during the entire captive period (n = 7); b) C-S-T: sheared immediately at capture and prior to transportation to the holding facility; thus the effects of capture and shearing were acting together (n = 6); c) C-T-S12: sheared after 12 days in captivity with the aim of allowing the animals to recover from the initial stress of capture and transport (n = 6). The shearing experiment conducted on day 12 compares animals that were not shorn with shorn animals; both groups were handled in the same way during the same period in captivity. This design seeks to minimise the confounding effects of capture and transport on the effect of shearing (see Appendix). Because our approach involves in vivo sampling from unanaesthetised animals, stress associated with handling is a component of each treatment. At capture, and on days 1, 2, 4 and 12, blood samples were taken from each animal. In addition, rectal temperature, heart rate and respiratory rate were recorded daily. The haematological parameters were: packed cell volume (PCV), total white blood cell count (WBC), neutrophil count, lymphocyte count, eosinophil count, monocyte count, and neutrophil:lymphocyte ratio (N:L ratio). The biochemical assays on blood plasma were: blood glucose concentration (GLU), cortisol concentration (CORT), and activity levels of the serum enzymes creatine kinase (CK) and aspartate aminotransferase (AST). Blood sampling and analysis Blood samples were obtained by jugular venepuncture from the upper section of the neck (Urquieta & Rojas 1990; Fowler 1994), following Fowler’s guidelines for llamas, except that an upper neck patch was shaved and disinfected with an alcohol–iodine solution (Fowler 1998). The minimum amount of blood necessary was drawn, using 21 GX1 1/2'' UTW needles (Venoject®) and 5 ml blood tubes (Vacutainer®; Becton Dickinson, Franklin Lakes, NJ, USA) which contained ethylene diamine tetra-acetic acid (EDTA) and heparin, for haemogram and cortisol measurements, respectively (Schalm & Jain 1986; Kaneko et al 1997). Blood smears were prepared following standard procedures for sampling wild ungulates in the field, by placing a drop of fresh blood, using a glass capillary (of 75 mm/75 µl), onto a Marienfeld® slide and smearing with another slide (76 × 26 × 1 mm approximately; Fowler 1986; Rhiney 1982). The smear was fixed with methanol and the slide labelled with a graphite pencil, in preparation for Giemsa staining and differential white blood cell counts (Coles 1980; Schalm & Jain 1986). These counts were carried out using standard procedures in the Veterinary School of the University of Chile (Coles 1980; Schalm & Jain 1986). Total white cell counts were undertaken for each sample in the field using a Neubauer® improved bright line camera (Precicolor of 0.100 mm by 0.0025 mm2) (Coles 1980; Schalm & Jain 1986). Under the extreme and remote field conditions of the study area, no automatic blood counter was available. Plasma was extracted by centrifugation and stored in a nitrogen tank within 2 h of collection for further enzyme and cortisol analysis. The same researcher performed all measurements in the field and the laboratory. 390
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Plasma cortisol concentration was measured using radioimmunoassay following WHO guidelines (Hall 1978) in the Endocrinology Laboratory of the Faculty of Biological Sciences (Pontificia Universidad Católica de Chile — a registered laboratory in the WHO programme of matched reagents and laboratory techniques for reproductive studies [Zekan & Ezcurra 1998]). The cortisol level was measured directly in aliquots of 50 µl of plasma diluted with 0.1M phosphate-buffered saline with pH 7.4, and heated to 60°C. The standard antibody, tracer and methodology were provided by the WHO matched reagent programme (Hall 1978; Zekan & Ezcurra 1998). The antibody is raised in rabbits and has a sensitivity of 10.5 nmol l–1. It cross-reacts with cortisol (100%), cortisone (25%), corticosterone (2.2%), 11-deoxycortisol (40%), 17-hydroxyprogesterone (10%), progesterone (0.5%), and 11-hydroxyprogesterone (
